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{ An E>l.amination of the concept of Arousal within the Context of the Sexual Behaviour of the snail, Helix aspersa Shelley A. Adamo Department of Biology McGill university, Montreal April, 1990 A thesis submitted te the Faculty of Graduate Studies and Research of McGill University in partial fulfillment of the requirements for the degree of Ph.D. @shelley Adamo, 1.990 .------------------------- ._--_. 2 ( Ta my parents, with love and gratitude for aIl their support and encouragement 3 Abstract Sexual 'arousal' in Helix aspersa can be divided into 2 components, sexual proclivity (the tendency of a snail to respond to conspecific contact with courtship) and sexual arousal (the intensity with which the snail courts) . Sexual proclivity and sexual arousal have different effects on feeding and locomotion and are differentially affected by sexual isolation, daily conspecific contact, and by a courtship pheromone found in the digitiform gland mucus. Therefore sexual arousal and sexual proclivity ara probably mediated by 2 separate ph}rsiological mechanisms. Behavioural state, or the animal' s general level of activity, correlates positively with mating behaviour. However, al though a central system controlling behavioural state probably exists, it has no direct effect on either sexual proclivity or sexual arousal. Confusion over the term 'arousal', which impedes neuroethological research in this area, would be decreased by the adoption of the terms used in this thesis. 4 Résumé "L'éveil" sexuel chez Hf'lix aspersa peut être divisé en deux composantes: la disposition sexuelle (soit la tendance d'un escargot à faire la cour lors d'un contact avec un congénère), et la stimulation ou l'éveil seyuel proprement dit (c'est-à-dire l'intensité avec laquelle l'escargot fait la cour). Non seulement la disposition et l'éveil sexuels ont-ils des effets distincts sur les comportements d'alimentation et de locomotion, mais ils sont affectés de manière différente par l'isolation sexuelle, le contact quotidien avec les congénères 1 et par une phéromone rel iée au comportement de cour que l'on trouve dans le mucus des glandes multifides. Il est donc fort probable que la disposition sexuelle et l'éveil sexuel soient servis par deux mécanismes physiologiquement distincts. L' étât comportementa l (l e ni veau général d' activi té de l'animal), est en corrélation positive avec le comportement d' appariement. Cependant, bien qu'il soit possib.le qu'un système central contrôlant l' étât comportemental existe, celui-ci s'avère sans effet, autant sur la disposition sexuelle que sur l'éveil sexuel. La confusion règnante en ce qui concerne le terme "éveil", et qui de fait freine la recherche en neuroéthologie dans ce domaine, se trouverait diminuée si l'on adoptait les termes utilisés dans cette thèse. 5 Preface The research presented in this thesis, and the preparation of the thesis i tself, are solely the work and responsibil i ty of the candidate. However, in the experiments requiring blind contraIs, Barbara Tolloczko, Caroline Tidd and Shelley LaBerge assisted with the data collection. The thesis chapters which have been publ ished, or have been submitted for pUblication, are listed below: Chapter 2. Adamo, S.A. and Chase, R. (1988), Canadian Journal of Zoology, 66: 1446-1453. Chapter 3. Adamo, S.A. and Chase, R. (in press), Journal of Experimental Zoology. Chapter 4. Adamo, S.A. and Chase, R. (in press), Behavioral and Neural Biology. Chapter 5. Adamo, S.A. and Chase, R. (in press), Behavioural and Neural Biology. Chapter 6. Adamo, S.A. and Chase, R. (submitted), Behavioural and Neural Biology. Chapters 2, 3, 4, 5, and 6 are in the formats required of them by their respective journals. Chapter 1 gi ves a general introduction to the topic and outlines the scientific problem addressed in this thesis. The discussion (Chapter 7) surnmarizes the resu1 ts of the thesis in the context of the scient i fic ," question posed in the introduction. 6 ( Contributions to Original Knowl.eoge Below is a listing of the main contributions to original knowledge contained in this thesis: 1) The thesÜ; gives a clear description of Helix aspersa sexual behaviour and copulation (Chapter 2) which previously had been poorly characterized. :2) It presents the f irst known function for dart shooting behaviour (Chapter 3) . It demonstrates that the digitiform gland mucus, which coats the dart, contains a courtship pheromone. 3) It establishes that the phenomenon of 'arousal' can be divided into 2 distinct components, arousal and proclivity (Chapter 4, Chapter 5) and that this division can be usefully applied to other molluscs (Chapter 7). 4) It demonstrates that the relationship between sexual behaviour and feeding behaviour in Helix can best be described as a time-sharing arrangement (Chapter 5). This is the first time that this complex behavioural interaction has been shown in a mollusc. 5) It clarifies the meaning of the term central 1 arousal' (Chapter 6). Chapter 7 shows that much of the controversy in the literature dealing with central 1 arousal' is due to a confusion in tenninology. clarify ing the term 1 arousal' will aid neuroethologists in their study of motivated behaviours. 7 The following statement is added in accordance with the regulations of the Facul ty of Graduate Studies and Research of McGill University: The candidate has the option, subject to the approval of the department, of including as part of the thesis the text, or duplicated published text (see below), of an original paper, or papers. In this cas~ the thesis must still conform ta all other requirements explained in Guidelines Concerning Thesis preparation. Additional material (procedural and design data as well as descriptions of equipment) must be provided in sufficient detail (e.g. in appendices) to allow a clear and precise j udgemen t to be made 0 f the importance and originality of the research reported. The thesis should be more than a mere collection of manuscripts published or to be published. It must include a general abstract. a full introduction. and literature review and a final overall conclusion. Connecting texts which provide logical bridges between different manuscripts are usually desirable in the interests of cohesion. It is acceptable for thesis to include as chapters authentic copies of papers already published, provided these are duplicated clearly on regulation thesis stationery and bound as an integral part of the thesis. Photographs or other materials which do not duplicate well must be included in their original forme In such instances. connecting texts are mandatory and supplementary explanatory material is almost always necessary. The inclusion of manuscripts co-authored by the candidate and ethers is acceptable but the candidate is required te rnake an explici t statement on who contributed to su ch work and to what extent, and supervisors must attest to the accuracy of the claims, e.g. before the Oral Committee. Since the task of the Examiners is made more difficult in these cases, i t is in the candidate' s interest to make the responsibilities of authors perfectly clear. Candidates fellowinq this option must inform the department before it submits the thesis for review. { 8 Acknowledgements Although it is established etiq.lette to thank one's supervisor for his time and expertise, my thanks to Dr. Ronald Chase are sincerely warm and heart-fel t. He has always been support ive of me and my research. His keen ability to analyze, and his own integrity and imagination as a scientist, has provided me with an invaluable learninq experience. I would also like to thank the members of my supervi::;ory committee, Dr. Valerie Pasztor, Dr. Gerry Pollack, and Or. Henry Reiswiq for their encouragement and constructive criticisms. l would like to thank Robert Lamarche and Guy L' Heureux for their advice and expert technical assistance with the photographie materials and with the laser printer. l would also like to thank Matthias Schmidt for his clear and literate translations of Meisenbeimer (1912) and Syzmanski (1913). l thank the Natural Sciences and Engineering Research Council of Canada for their financial support. l would also like to thank my colleagues in the Chase Lab., especially Holly Bradshaw and Barbara Tolloczko, for their constant encouragement and for their qifts of both time and expertise. Finally l would like to thank my relatives and friends, especially my parents and Jim Belanqer, who { were always willing to listen. - 9 Table of Contents Page Abstract ........................................ 3 Résumé •..••••.•••...•••..•••••..••••..••••...••. 4 Preface .......................................... 5 Acknowledqements •...•••...•••..•.•••...••.....•• 8 Chapter 1. Thesis Introduction ..••....•.....•.. 10 Chapt.er 2. Courtship and Copulation in the Terrestrial snail, Helix aspersa 31 Chapter 3. The' Love Dart 1 of the Snail, Helix aspersa Inj ects a Pheromone that Decreases Courtship Duration •....•.. 52 Chapter 4. Dissociation of Sexual Arousal and Sexual Proclivity in the Garden Snail, Hel ix aspersa ................ 75 Chapter 5. The Interactions of Sexual Behaviour, Feeding Behaviour and Locomotion in the Behaviourt.l Hierarchy of the Snail l Hel ix aspersa .••....••....... 98 Chapter 6. 1 Central Arousal 1 and Sexual Responsiveness in the snail, Helix jJlpersa ..•....••.•...••...•••.....•. 122 Chapter 7. Thesis Discussion •..••••..••••...••. 155 Bibl iography ...................................... 181 , ,~ { 10 Chapter 1. Thesis Introduction { 11 Introductory remarks on the snail« Helix aspersa Helix aspersa is a terrestrial snail found in many temperate parts of the world (Herzberg and Herzberg, 1962) . Its distribution is restricted by its need for high humidity and moderate temperatures. Possibly due to its sensitivity to dry air, H. aspersa tends to be most active at night. Snails are capable of aestiva":ing when conditions become adverse. A snail will withdraw into its shell and seal the opening with a membrane to retard moisture loss. By aestivating when conditions are poor, snails can survive for several years, reproducing annually (Potts, 1975; Bailey, 1981).
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